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Biology subjects

Longden, K. D.

Publications and source records attributed to Longden, K. D..

8 recordsLinked to original sources

Structured Connectivity Across Multiple Drosophila Mushroom Bodies

Learning and memory depend on plasticity within neural circuits, but the extent to which the underlying architecture of memory networks is stereotyped or structured remains unclear. Random connectivity may maximise stimulus discrimination, whereas structured connectivity could preferentially route behaviourally relevant information. Here, we compare five adult Drosophila melanogaster Mushroom Body (MB) hemispheres across three connectomes and establish a unified cross-connectome framework for uniglomerular projection neurons (uPNs), Kenyon Cells (KCs), Mushroom Body Output Neurons (MBONs) and Lateral Horn Centrifugal Neurons (LHCENTs). Despite variation in KC abundance and fine-scale connectivity, we identify reproducible organisation across the uPN[->]KC and KC[->]MBON pathways. Food-associated uPN channels consistently contact a greater proportion of KCs than expected by chance, and this bias is preferentially routed through KCs towards approach-promoting MBONs. Sensory input also remains stereotyped across sister MBONs from the same hemisphere despite variation in their individual KC partners. Finally, recurrent LHCENT feedback (predicted-inhibitory) preferentially targets KCs receiving these food-associated inputs. Together, these findings show that a memory network can accommodate local variability while preserving structured pathways that prioritise ethologically relevant sensory information.

neuroscience↗

Connectomic Analysis of Mitochondria in the Central Brain of Drosophila

Mitochondria are integral to the metabolism and cell biology of a neuron. Electron microscopy images of fly brain volumes, taken for connectomics, can be analyzed for mitochondria as well as the cells and synapses already reported. Here, from the Drosophila Hemibrain connectome dataset, we extract, classify, and measure approximately 6 million mitochondria, with the majority located among more than 20 thousand neurons and over 5500 cell types. Each mitochondrion is annotated with its location, orientation, voxel size, and appearance (dark and dense, light and sparse, or medium), and each synapse is linked to its closest mitochondrion. Using these data, we show how the most basic characteristics of mitochondria--volume, distance from synapses, and appearance--vary considerably between cell types and between brain regions. Mitochondria are larger and closer at presynapses than at postsynapses, and presynapses typically have a mitochondrion within one micron. However, cells important for learning and memory, Kenyon cells, have unusually small and sparse mitochondria that are placed with unusual precision near only half of presynapses. We find that mitochondria occupy a greater fraction of cell volume in inhibitory neurons than excitatory cells, dopaminergic neurons have a distinct synaptic positioning of mitochondria, and that glutamatergic neurons have a high fraction of mitochondria with a light appearance. We also find that synapses with more postsynaptic partners have larger presynaptic mitochondria and more distant postsynaptic mitochondria. Finally, we have extended the data model of our public web interface, neuPrint, to record our mitochondria data as searchable subcellular components of neurons in a connectomic database. These results indicate wide-ranging principles for how mitochondrial organization varies by cell type in a dataset of unprecedented size and coverage.

neuroscience↗

Connectome-driven neural inventory of a complete visual system

Vision provides animals with detailed information about their surroundings, conveying diverse features such as color, form, and movement across the visual scene. Computing these parallel spatial features requires a large and diverse network of neurons, such that in animals as distant as flies and humans, visual regions comprise half the brains volume. These visual brain regions often reveal remarkable structure-function relationships, with neurons organized along spatial maps with shapes that directly relate to their roles in visual processing. To unravel the stunning diversity of a complex visual system, a careful mapping of the neural architecture matched to tools for targeted exploration of that circuitry is essential. Here, we report a new connectome of the right optic lobe from a male Drosophila central nervous system FIB-SEM volume and a comprehensive inventory of the flys visual neurons. We developed a computational framework to quantify the anatomy of visual neurons, establishing a basis for interpreting how their shapes relate to spatial vision. By integrating this analysis with connectivity information, neurotransmitter identity, and expert curation, we classified the [~]53,000 neurons into 727 types, about half of which are systematically described and named for the first time. Finally, we share an extensive collection of split-GAL4 lines matched to our neuron type catalog. Together, this comprehensive set of tools and data unlock new possibilities for systematic investigations of vision in Drosophila, a foundation for a deeper understanding of sensory processing.

neuroscience↗

Passive inertial damping improves high-speed gaze stabilization in hoverflies

Gaze stabilization reflexes reduce motion blur and simplify the processing of visual information by keeping the eyes level. These reflexes typically depend on estimates of the rotational motion of the body, head, and eyes, acquired by visual or mechanosensory systems. During rapid movements, there can be insufficient time for sensory feedback systems to estimate rotational motion, requiring additional mechanisms. Solutions to this common problem are likely to be adapted to an animals behavioral repertoire. Here, we examine gaze stabilization in three families of dipteran flies, each with distinctly different flight behaviors. Through frequency response analysis based on tethered-flight experiments, we demonstrate that fast roll oscillations of the body lead to a stable gaze in hoverflies, whereas the reflex breaks down at the same speeds in blowflies and horseflies. Surprisingly, the high-speed gaze stabilization of hoverflies does not require sensory input from the halteres, their low-latency balance organs. Instead, we show how the behavior is explained by a hybrid control system that combines a sensory-driven, active stabilization component mediated by neck muscles, and a passive component which exploits physical properties of the animals anatomy--the mass and inertia of its head. This adaptation requires hoverflies to have specializations of the head-neck joint that can be employed during flight. Our comparative study highlights how species-specific control strategies have evolved to support different visually-guided flight behaviors. SIGNIFICANCE STATEMENTAcross the animal kingdom, reflexes are found which stabilize the eyes to reduce the impact of motion blur on vision--analogous to the image stabilization functions found in modern cameras. These reflexes can be complex, often combining predictions about planned movements with information from multiple sensory systems which continually measure self-motion and provide feedback. The processing of this information in the nervous system incurs time delays which impose limits on performance when fast stabilization is required. Hoverflies overcome the limitations of sensory-driven stabilization reflexes by exploiting the passive stability provided by the head during roll perturbations with particularly high rotational kine-matics. Integrating passive and active mechanisms thus extends the useful range of vision and likely facilitates distinctive aspects of hoverfly flight.

neuroscience↗

Synergy of color and motion vision for detecting approaching objects in Drosophila

Color and motion are used by many species to identify salient moving objects. They are processed largely independently, but color contributes to motion processing in humans, for example, enabling moving colored objects to be detected when their luminance matches the background. Here, we demonstrate an unexpected, additional contribution of color to motion vision in Drosophila. We show that behavioral ON-motion responses are more sensitive to UV than for OFF-motion, and we identify cellular pathways connecting UV-sensitive R7 photoreceptors to ON and OFF-motion-sensitive T4 and T5 cells, using neurogenetics and calcium imaging. Remarkably, the synergy of color and motion vision enhances the detection of approaching UV discs, but not green discs with the same chromatic contrast, and we show how this generalizes for visual systems with ON and OFF pathways. Our results provide a computational and circuit basis for how color enhances motion vision to favor the detection of saliently colored objects.

neuroscience↗

Impact of walking speed and motion adaptation on optokinetic nystagmus-like head movements in the blowfly Calliphora

The optokinetic nystagmus is a gaze-stabilizing mechanism reducing motion blur by rapid eye rotations against the direction of visual motion, followed by slower syndirectional eye movements minimizing retinal slip speed. Flies control their gaze through head turns controlled by neck motor neurons receiving input directly, or via descending neurons, from well-characterized directional-selective interneurons sensitive to visual wide-field motion. Locomotion increases the gain and speed sensitivity of these interneurons, while visual motion adaptation in walking animals has the opposite effects. To find out whether flies perform an optokinetic nystagmus, and how it may be affected by locomotion and visual motion adaptation, we recorded head movements of blowflies on a trackball stimulated by progressive and rotational visual motion. Flies flexibly responded to rotational stimuli with optokinetic nystagmus-like head movements, independent of their locomotor state. The temporal frequency tuning of these movements, though matching that of the upstream directional-selective interneurons, was only mildly modulated by walking speed or visual motion adaptation. Our results suggest flies flexibly control their gaze to compensate for rotational wide-field motion by a mechanism similar to an optokinetic nystagmus. Surprisingly, the mechanism is less state-dependent than the response properties of directional-selective interneurons providing input to the neck motor system.

animal behavior and cognition↗

Synaptic targets of functionally specialized R7 and R8 photoreceptors in the central eye and dorsal rim area of Drosophila

Color and polarization provide complementary information about the world and are detected by specialized photoreceptors. However, the downstream neural circuits that process these distinct modalities are incompletely understood in any animal. Using electron microscopy, we have systematically reconstructed the synaptic targets of the photoreceptors specialized to detect color and skylight polarization in Drosophila, and we have used light microscopy to confirm many of our findings. We identified known and novel downstream targets that are selective for different wavelengths or polarized light, and followed their projections to other areas in the optic lobes and the central brain. Our results revealed many synapses along the photoreceptor axons between brain regions, new pathways in the optic lobes, and spatially segregated projections to central brain regions. Strikingly, photoreceptors in the polarization-sensitive dorsal rim area target fewer cell types, and lack strong connections to the lobula, a neuropil involved in color processing. Our reconstruction identifies shared wiring and modality-specific specializations for color and polarization vision, and provides a comprehensive view of the first steps of the pathways processing color and polarized light inputs.

neuroscience↗

Spike interval coding of translatory optic flow and depth from motion in the fly visual system

Many animals use the visual motion generated by travelling in a line, the translatory optic flow, to successfully navigate obstacles: near objects appear larger and to move more quickly than distant ones. Flies are experts at navigating cluttered environments, and while their visual processing of rotatory optic flow is understood in exquisite detail, how they process translatory optic flow remains a mystery. Here, we present novel cell types that have motion receptive fields matched to translation self-motion, the vertical translation (VT) cells. One of these, the VT1 cell, encodes forwards sideslip self-motion, and fires action potentials in clusters of spikes, spike bursts. We show that the spike burst coding is size and speed-tuned, and is selectively modulated by parallax motion, the relative motion experienced during translation. These properties are spatially organized, so that the cell is most excited by clutter rather than isolated objects. When the fly is presented with a simulation of flying past an elevated object, the spike burst activity is modulated by the height of the object, and the single spike rate is unaffected. When the moving object alone is experienced, the cell is weakly driven. Meanwhile, the VT2-3 cells have motion receptive fields matched to the lift axis. In conjunction with previously described horizontal cells, the VT cells have the properties required for the fly to successfully navigate clutter and encode its movements along near cardinal axes of thrust, lift and forward sideslip.

neuroscience↗